January 10, 2014

Natural selection on human Y chromosomes

I am not quite sure what the analyses of this paper actually show. Neither migration nor admixture are mentioned in the text, and, in my opinion, these processes have shaped modern human Y chromosomal variation.

Migration may result in the expansion of a successful set of Y chromosome lineages, while admixture between divergent populations may inflate estimates of diversity in a population. The Complete Genomics data is dominated by two haplogroups representing vary recent expansions in Europe and West Africa. Is the expansion of R-M269 in Europe an example of selection or large-scale replacement? What does it mean to model "Europeans" or "Africans" as single evolving populations, when both of these were likely formed over the last few thousand years by admixture of divergent pre-existing populations.

PLoS Genetics doi:DOI: 10.1371/journal.pgen.1004064

Natural Selection Reduced Diversity on Human Y Chromosomes

Melissa A. Wilson Sayres et al.

The human Y chromosome exhibits surprisingly low levels of genetic diversity. This could result from neutral processes if the effective population size of males is reduced relative to females due to a higher variance in the number of offspring from males than from females. Alternatively, selection acting on new mutations, and affecting linked neutral sites, could reduce variability on the Y chromosome. Here, using genome-wide analyses of X, Y, autosomal and mitochondrial DNA, in combination with extensive population genetic simulations, we show that low observed Y chromosome variability is not consistent with a purely neutral model. Instead, we show that models of purifying selection are consistent with observed Y diversity. Further, the number of sites estimated to be under purifying selection greatly exceeds the number of Y-linked coding sites, suggesting the importance of the highly repetitive ampliconic regions. While we show that purifying selection removing deleterious mutations can explain the low diversity on the Y chromosome, we cannot exclude the possibility that positive selection acting on beneficial mutations could have also reduced diversity in linked neutral regions, and may have contributed to lowering human Y chromosome diversity. Because the functional significance of the ampliconic regions is poorly understood, our findings should motivate future research in this area.

18 comments:

"Migration may result in the expansion of a successful set of Y chromosome lineages, while admixture between divergent populations may inflate estimates of diversity in a population."True, though over time migration and admixture reduce to mere seeding events. Numbers are no protection against selective disadvantages, even though it may help some lineages to persist over a longer period. The selective advantage of eg. YDNA R, whatever the cultural trigger, is strongly suggested by its wave-like distribution that even includes west Africa, its proliferation among Native and Black Americans and its apparent Late Neolithic replacement of once much more diverse West European YDNA I. However, I figure migration may also impose a new cultural parameter on alien territories what may help the expansion of lineages amongst populations that previously remained exempt of these same haplogroups, despite thousands of years regional coexistence: YDNA I and YDNA R already existed for tens of millennia, and even the ANE-admixed Motala scandinavians still didn't show a trace of YDNA R. This cultural factor can't be dismissed lightly, since where most of the ancient YDNA I lineages became extinct in Northwestern Europe, eg. I2a1b remained higly diverse (though rare) in Britain while a single lineage managed to thrive in Eastern Europe. A simple explanation might be that I2a1b was seeded in Eastern Europe by migration and turned out to have a selective advantage within the new cultural reality. Elsewhere, those same migrant YDNA I lineages were most likely to disappear if they came in low numbers and without cultural or natural advantage. An alternative migration scheme based on natural selection and seeding may propose a single population where R1b and R1a dominated, as already attested in Beaker populations of northern continental Europe, that was in close contact with I2a1b and expanded in different directions, including the Mediterranean (R1b) and the Adriatic Sea (I2a1b), while another mutational cline towards the east can be perceived for R1a. Actually, I already did a long time ago.

Natural slection obviously reduces the diversity of Y chromosome because the selection is based on the autosomal genome and Y-chromosome is passive and remains mostly unchanged.

"While we show that purifying selection removing deleterious mutations can explain the low diversity on the Y chromosome, we cannot exclude the possibility that positive selection acting on beneficial mutations could have also reduced diversity in linked neutral regions, and may have contributed to lowering human Y chromosome diversity."

Admixture of course has it's own effect, but can we understand the admixture process being unattached from the natural selection as a systematic phenomenon?

"Is the expansion of R-M269 in Europe an example of selection or large-scale replacement?"

Basically large-scale replacement, although replacement was by no means complete obviously.

"Alternatively, selection acting on new mutations, and affecting linked neutral sites, could reduce variability on the Y chromosome".

I think the authors make the mistake of assuming all 'selection' is genetic. If a particular Y-chromosome is closely associated with some improved technology than obviously that Y-DNA will expand at the expense of other Y-DNAs.

"we show that low observed Y chromosome variability is not consistent with a purely neutral model".

Of course not.

"Instead, we show that models of purifying selection are consistent with observed Y diversity".

But that 'purifying selection' need not be genetic selection. Technological or cultural selection would achieve the same result.

"its [YDNA R] proliferation among Native and Black Americans"

Cultural advantage within the particular society surely rather than any genetic advantage.

"its apparent Late Neolithic replacement of once much more diverse West European YDNA I".

Surely technologial rather than genetic advantage once more.

"Admixture of course has it's own effect, but can we understand the admixture process being unattached from the natural selection as a systematic phenomenon?"

Yes. Admixture would be a very major driver of genetic evolution, allowing selection to operate on new genetic combinations. That is what plant and animal breeding is mainly based on.

"Yes. Admixture would be a very major driver of genetic evolution, allowing selection to operate on new genetic combinations. That is what plant and animal breeding is mainly based on. "

Of course, I do understand this. My idea was to consider admixture being part of natural selection. Of course we can assume that migrations preceding admixtures can lead also to a deteriorating process, but in a long run evolution have to be positive and we can include admixture to the natural selection of species. So it can't be unattached. This was my question.

But admixture events are accidental, depending on what populations are available in a particular region to admix. Dienekes' post on the SLC24A5 mutation show admixture gave rise to that mutation but it was only possible because populations containing the C3 and C10 mutations mixed with each other.

"in a long run evolution have to be positive and we can include admixture to the natural selection of species".

It so important to understand that selection in humans may have nothing to do with deleterious or advantageous traits. All one needs to do is look at how selection has worked in dog morphology to realize that when humans are involved, the direction of genetic change can have more to do with fashion than with function. The other point is that a truly deleterious trait can occur in all shapes and forms, mainly because of microbes, but also because of human nutritional needs. Otherwise very adaptive strains humans could very well have disappeared because of a simple lack of specific immunity.In thinking about this, it is really helpful to remember Ecclesiastes 9:11:"I returned, and saw under the sun, that the race is not to the swift, nor the battle to the strong, neither yet bread to the wise, nor yet riches to men of understanding, nor yet favor to men of skill; but time and chance happeneth to them all. "

"Basically large-scale replacement, although replacement was by no means complete obviously."

Aren't the recent papers starting to undermine that a bit i.e. the EEF population being itself admixed between first farmers and WHG?

(Although there could have been two large-scale replacements - a first farmer one followed by a later herder over-run which partially disguises the first.)

I guess it's perfectly possible for y dna to be largely replaced disproportionately but isn't the weighting now at mostly continuous (if you include the admixed portion of WHG inside EEF) rather than mostly replaced?

Unknown, I think that we can't compare dog breeds to any other species. Dogs are a result of fully artificial breeding. When a dog pack becomes a part of wilderness again and starts to live like wolves they also start to normalize to the original form. There is of course exceptions in the nature everywhere, local and temporary exceptions, but it doesn't make the natural selection meaningless. Maybe humans can control genes in the future and understand what is best for them. Maybe not. It is not anymore natural selection. But even our species has been controlled by the natural selection, our brains are not an exception. Only becoming smarter we have succeeded to multiply as much as the history proves. There has been substantive mutations, but it doesn't explain how Homo Sapiens succeeded to spread everywhere.

Fanty"My guess is, thats why there is this realtively huge difference between the results of ADMIXTURE and a MDS."

Yes, I think the labels chosen for the components are slightly misleading some people.

A population that is made up of one half which is 100% component A and a second half which is 50% component A and 50% component B could be described as 75% A + 25% B or (if you define the second population as component C) as 50% A + 50% C.

Both are valid as historically it is relevant when and how C was formed but people need to remain aware that C is a composite.

If what Fanty wrote below is correct, it shows how much the concept of admixture changes the historical picture. These are very different results and one of them is inaccurate in terms of describing what happened between then and now.And that's what the test should be -- accuracy in describing what happened back then. The ancient DNA in northern Europe simply doesn't support a continuous in situ hunter gatherer in most of northern Europe. -- SL

"Fanty said...ADMIXTURE claims the only places in Europe where WHG anchestry is greater than EEF anchestry are Scottland, Finland, the baltic states and surounding.MDS claims all of Europe more north than the alps is more WHG than EEF. (or better: has more "exclusively WHG alleles" than "exclusely EEF alleles")Explanation:MDS compared WHG to EEF and excludes all alleles than both share (the WHG admixure in EEF would be excluded by this)"

mikej2 said...“Unknown, I think that we can't compare dog breeds to any other species. Dogs are a result of fully artificial breeding.”

Mike, I walk into the typical American supermarket, and from one end to the other, the animals and plants are products of “artificial selection.” The physical morphology and often the genetics are quite distant from the wild forms, right down to the “cultured” microbes in the cheeses. The only thing that should be wild in 10,000 items are Atlantic flounder filets and some kind of tuna, and I can’t even vouch for that. We left natural selection behind a long time ago, at least with regard to our food supply.

“When a dog pack becomes a part of wilderness again and starts to live like wolves they also start to normalize to the original form.” No, dogs make terrible wolves. They don’t revert to original form. They basically live off garbage on the fringes of human areas. They are not very good at living off wild prey. Cats are different. But cats are really weird.

“Only becoming smarter we have succeeded to multiply as much as the history proves. There has been substantive mutations, but it doesn't explain how Homo Sapiens succeeded to spread everywhere.”

But what makes us “smarter” is an interesting question. I am sitting at a computer right now and typing a message in one of many human languages. Other plants and animals can’t do that. But the computer was built on the other side of the earth and I have no idea of how to build one from scratch. Where would I mine the chromium or purify the silicon? Would I have to invent an alphabet? Who else would be able to read it?

Alphabets are only about 3000 years old and “we” only came up with computers in the last 70 years. If we were genetically “smarter” why didn’t we come up with this stuff 40,000+ years ago? In fact, why did it take us so long to come up with frozen pizza, chicken mcnuggets and canned dog food? 10,000 years ago most humans were living in caves and living on wild nuts and berries and digging up clams. What took so long?

Grey said...@Unknown"The ancient DNA in northern Europe simply doesn't support a continuous in situ hunter gatherer in most of northern Europe"

'I think the key phrase there is "in situ." It's more a case of a tide going out and then back in again.'"

I think you are right. But maybe the tide came in and out all the time. "Hunter-Gatherers" creates an unfortunate limitation on what these people did. For example, fishing is HG -- so who had the boats to hire? And if you had enough deer meat or fish, wouldn't you sell it to the farmers? We don't really have a sense from archaeology of how the seasons and the marketplaces affected the ebb and flow of peoples. Or mixed them. Ancestral cemeteries may have us looking at old guard who were claiming the land, not the permanently transient. Eg, D's notion that cremation was a way of taking your dead with you wherever you happened to go.

GENERAL COMMENTWhat is called "natural selection" is rarely such! The rape, pillaging, forced conversions and villages benefitting from survival, though, in all points are view, are the primary reasons we see what we see. Now we pretend that because of what is named admixture, this is voluntary when in fact, they are consequences of states undergoing change and in the process, stuff just is! There is no more less Muslim fundamentalism in European Turkey (former Byzantium) than DNA evidence to a conversion process (religion) upon an Eastern European loci, be it Serb, Croat, Greek, etc) and their Mamluk brothers, who accepted their fate and were forced to survive by any means necessary.

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